Brain Sci. 2012, 2, 1-21; doi:10.3390/brainsci2010001

brain sciences ISSN 2076-3425

www.mdpi.com/journal/brainsci/

Review

Why the Brain Knows More than We Do: Non-Conscious Representations and Their Role in the Construction of Conscious Experience

Birgitta Dresp-Langley

Centre National de la Recherche Scientifique, UMR 5508, Université Montpellier, Montpellier 34095,

France; E-Mail: birgitta.dresp-langley@univ-montp2.fr; Tel.: +33-(0)4-67-14-45-33;

Fax: +33-(0)4-67-14-45-55

Received: 16 November 2011; in revised form: 12 December 2011 / Accepted: 20 December 2011 /

Published: 27 December 2011

Abstract: Scientific studies have shown that non-conscious stimuli and representations

influence information processing during conscious experience. In the light of such evidence,

questions about potential functional links between non-conscious brain representations and

conscious experience arise. This article discusses neural model capable of explaining how

statistical learning mechanisms in dedicated resonant circuits could generate specific

temporal activity traces of non-conscious representations in the brain. How reentrant

signaling, top-down matching, and statistical coincidence of such activity traces may lead

to the progressive consolidation of temporal patterns that constitute the neural signatures of

conscious experience in networks extending across large distances beyond functionally

specialized brain regions is then explained.

Keywords: non-conscious representation; temporal brain activity patterns; top-down

matching; reentrant signaling; resonance; conscious experience

1. Introduction

During early childhood, our brain learns to perceive and represent the physical world. Such

knowledge is generated progressively over the first years of our lives and a long time before we

become phenomenally conscious of the Self and its immediate or distant environment [1]. Statistical

learning, or the implicit learning of statistical regularities in sensory input, is probably the first way

through which humans and animals acquire knowledge of physical reality and the structure of

continuous sensory environments. This form of non-conscious learning operates across domains,

OPEN ACCESS

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across time and space, and across species, and it is present at birth when newborns are exposed to and

tested with speech stream inputs [2]. Conscious experience kicks in much later in life, involving

complex knowledge representations that support conscious thinking and abstract reasoning [3–5]. How

is information represented and processed in the brain to enable such experience? To be able to answer

this question, we need to understand how structured knowledge can be represented in neural circuits.

Brain representations have been conceptually divided [6–8] into functionally segregated conscious

and non-conscious worlds generating different forms of cognition and awareness. How the different

cognitive worlds interact to produce successful adaptive behavior at the least possible cost is not known,

but a large number of studies have shown that non-conscious brain processes influence perceptions and

representations embedded in ongoing conscious experience. Non-conscious brain processes have the

capacity of encoding vast amounts of information relative to complex events of the physical world

through multiple interdependent sensory channels at any given moment of time. Conscious processing,

on the other hand, is extremely limited in capacity, which explains why most of our knowledge of the

world is generated outside consciousness [9]. Whenever we consciously remember, decide, or act, our

brain seems to “know” far more about what we are doing and why we are doing it than our conscious

experience is able to consider. It appears that, as a result of evolutionary pressure and selection, the

human brain has achieved to govern complexity at the least possible cost by selectively allocating

resources, at the level of our sensations, emotions, decisions, and actions.

Theoretical models have tried to explain how such a selective process may work by suggesting that

non-conscious sensorial and representational processes interact, through working and long-term memory,

to generate brain learning and, ultimately, enable conscious experience [10–13]. Some of these have

defended the idea that non-conscious signals and memory representations are selectively made available

to conscious experience on the basis of temporal coincidence of representations at a given moment in

time. This would involve neural mechanisms that match distributed signals from non-conscious and

conscious levels of brain processing into time dependent representations of knowledge and events. On

the grounds of functional hypotheses of these and earlier theories [14–16], it is possible to clarify some

major functional implications of non-conscious brain representation for the generation of conscious

experience: (1) Only non-conscious brain processes have enough capacity to process the complex

cross-talk between signals originating from various simultaneously activated and functionally specific

sensory areas; (2) The temporal signatures of conscious experience are formed and consolidated in

reverberating interconnected neural circuits that extend across long distances and well beyond

functionally specific brain regions; (3) This is achieved though the matching of coincident neural

activity traces of non-conscious memory representations; (4) The temporal signatures of conscious

experience are independent from spatial brain maps and remain available after destruction of the

specific functional circuits through which they have been originally formed.

The following section presents evidence which supports the general idea defended here that

non-conscious brain representation enables a selective process for either making representations

accessible to, or suppressing them from, immediate consciousness. Then, Section 3 introduces some of

the major functional assumptions of a brain model capable of explaining how such a selective process

could work, and Section 4 clarifies how temporal neural signatures of conscious experience could be

generated on the basis of non-conscious brain processing. In Section 5, a conclusion and further

perspectives are given.

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2. Non-Conscious Perception Influencing Conscious Cognition and Action

Non-conscious processes in emotional, perceptual and cognitive function cover a wide range of

observations, such as subliminal psychodynamic activation and non-conscious perception in hypnosis,

subliminal semantic priming, effects of stimuli that are not consciously perceived on recognition

processes, implicit learning, the perceptual integration of subliminal luminance or color targets , and

phenomena of blind-sight in patients with striate cortical lesions, non-human primates, and normal

observers Subliminal psychodynamic activation or SPA [17] describes behavioral effects where the

exposure to subliminally presented, drive-related stimuli results in a positive change in the emotional

and mental state of human observers [17,18]. So-called “symbiotic” imagination or fantasies, where

comforting internal representations are triggered by comforting subliminal stimulation, for example,

are key issues here. Results from clinical studies have shown that subliminal verbal messages designed

to induce such symbiotic fantasies and administered under double-blind quasi-experimental conditions

significantly reduce anxiety levels and raise the motivation of psychiatric patients such as drug

abusers [19]. Follow-up examinations furthermore revealed that the experimental patient groups who

received treatment with the subliminal stimuli reported more dreams containing positive symbiotic

events than the controls. It is emphasized that the non-conscious character of the stimuli in subliminal

psychodynamic activation (SPA) is critical: effects produced under conditions where observers are

unaware of the nature and content of the stimuli were found to be significantly stronger than those

produced by the same stimuli presented at supraliminal levels [20]. Explanatory models of SPA effects

suggest that supraliminal stimuli lose some of their power to produce the desired effects on internal

representations because subjects perceive them as part of an externally administered procedure [21]. In

other words, stimulus awareness would in this case diminish the organisms’ capacity for responding

efficiently to drive- and affect-related stimuli. Some restricting effect of awareness on psychodynamic

responsiveness is widely believed to diminish the efficiency of relaxation techniques that combine

soothing music with verbal suggestions, which has lead to the sustained use of subliminal suggestions

combined with soft music in relaxation therapy. Experimental studies have shown that the most

efficient combinations appear to be indeed those where soft music is presented together with verbal

stimuli of intensities below the level of conscious perception [22].

Theory and findings regarding SPA effects have received critical feed-back raising issues relating to

the appropriateness of control and threshold stimuli in the various experiments [23,24], the possible

need for physiological indicators of anxiety reduction such as the subject’s heart rate in addition to

the psychological measures [25], and questions about the need for neutral, i.e., neither drive- nor

affect-related, stimuli to establish individual subjective thresholds for SPA [26]. However, quantitative

and qualitative reviews and meta-analyses of research conducted over the years lead to the conclusion

that the major findings remain statistically significant [27]. Partial-cue hypotheses, which suggest that

some structural cues in subliminal stimuli might be directly available to consciousness and therefore

explain SPA effects, have been put into question [20].The implications of the initial observations

for cognitive science remain the same: conscious processing interferes with responding optimally to

drive- and affect-related stimuli.

Hypnosis and hypnotic suggestibility are phenomena that are not yet fully understood scientifically,

but merit nonetheless attention. Hypnotic induction is not as such a subliminal process since the

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psychodynamic effects in this case are mediated via essentially supraliminal verbal suggestions.

Hypnotic phenomena may reflect states of altered consciousness [28], and the degree to which a

human individual may respond to hypnotic suggestions is referred to as hypnotic susceptibility, which

can be accurately predicted on the basis of psychometric tests such as the Waterloo-Stanford Group

Scale of Hypnotic Susceptibility [29,30]. Hypnotic susceptibility is an estimate of the ability of a man

or a woman to enter some trance-like state where overall awareness is shifted away from the general

context and environment, and focused on the symbiotic fantasies induced by the hypnotic (verbal)

suggestions of an expert clinician. Hypnotic suggestibility in young men and women has been shown

to be significantly enhanced following application of weak (one micro Tesla) burst-firing magnetic

fields for 20 min over the temporal-parietal lobes of the right hemisphere [31]. This suggests that the

signatures of the low-frequency magnetic fields contain bio-relevant information which directly affects

the neural processes underlying hypnotizability. Positron emission tomography (PET) measures of

regional cerebral blood flow and electroencephalographic (EEG) measures of brain electrical activity

have shown that specific patterns of cerebral activation are associated with the hypnotic state and

the processing of hypnotic suggestions [32]. Another PET study comparing highly susceptible males

with an additional ability to hallucinate under hypnosis, so-called “hallucinators”, to other highly

hypnotizable “non-hallucinators” revealed that a specific region in Brodman area 32 was activated in

the group of “hallucinators” when they heard an auditory stimulus, or when they merely hallucinated

hearing it under hypnosis [33]. Such activation was absent when the “hallucinators” merely imagined

hearing the tone, and in all “non-hallucinators” regardless of experimental condition.

Measurable consequences of hypnosis intervention on cognitive function were also reported. With

highly susceptible observers, hypnosis may produce an inhibition of correct responses in perceptual

tasks with conflicting stimuli [34], correlated with significant changes in cortical evoked potentials.

Effects of hypnotic susceptibility on auditory event-related potentials (AERPs) were found in

observers who were instructed to ignore tones while accomplishing some other task, such as reading a

novel. The highly hypnotizable subjects revealed different AERP amplitudes and latencies when

ignoring the tones, and were significantly slower in responding to the not-to-be-attended stimuli

compared with less susceptible subjects. This suggests that highly hypnotizable humans may have a

greater ability to shift awareness towards relevant stimuli and away from irrelevant ones [35].

Furthermore, specific hypnosis techniques such as suggested selective deafness or selective

visualization appear to influence learning processes in the desired direction, which means that subjects

under hypnosis are able to eliminate from consciousness exactly what they are told to [36].

A particular example showing how supraliminal perceptions or representations may become

subliminal through guided shifts in awareness induced by hypnotic suggestions is the hypnotic control of

physical pain, or hypnotic analgesia [37,38]. Research on hypnotic analgesia has grown substantially

in recent years and helped to develop strategies for acute and chronic pain management in the private

and public domains. Although it is often difficult to distinguish facts from artifacts such as placebo,

current knowledge points towards the general agreement that pain and distress perception is

significantly lowered through hypnosis, in acute as well as chronic pain patients with high hypnotic

susceptibility [39]. Recent scientific studies have investigated the effect of hypnotically induced

obstructive fantasies, targeted at eliminating painful stimuli from consciousness. The results showed

significantly higher pain and distress tolerance, significant changes in EEG amplitude, and a significantly

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reduced heart rate [40] in highly susceptible individuals subjected to painful electrical stimulation under

hypnosis. Target specific amplitude peaks in response to somatosensory stimuli were found significantly

reduced in subjects with high hypnotizability in a pain target detection task [41]. Apart from the possible

implications for clinical research, these effects of hypnosis suggest that perceptions and representations

embedded in ongoing awareness can be selectively eliminated from consciousness [38].

Effects where a person’s conscious feelings, judgment, or choices are changed by non-conscious

processing of images or messages have also been reported. Such is supposed to happen every time

when we watch television or look at colorful adverts in a magazine or in the street [42]. In a BBC

broadcast study by Underwood [43], faces were flashed subliminally within the program for about

20 ms in a restricted part of the network region. Immediately after the broadcast, TV viewers were

invited to make a judgment by telephone about a neutral, supraliminal face image that expressed no

emotion. Judgments were made by telephoning one of two numbers (1 or 2) indicating “sadness” or

“happiness”. Statistical analyses of the phone call responses revealed that viewers who received a

subliminal smiling face in the broadcast were less likely to judge the neutral face as being happy than

were those viewers who were not exposed to the subliminal image in the program. Underwood

suggested that this effect could be explained in terms of a contrast effect, where the neutral expression of

the supraliminal image is interpreted as “sadder” than the smiling subliminal image. However, the

broadcast study provided no information as to whether the so-called subliminal frames may have been

perceived in some cases. Attempts to replicate the results of the broadcast study under laboratory

conditions did not yield findings unambiguous enough to allow for a clear conclusion. Emotional

priming is often difficult to control and depends on a variety of factors, ranging from the graphic quality

of the material presented to the general mood of a given individual subject at a given moment. It can

therefore be expected that, when priming people with emotions, both contrast and assimilation effects

may occur. Also, some stimuli may have a particular status in subliminal emotional priming [44] given

that differences in the detection thresholds of different subliminal images or stimuli were reported,

with the lowest thresholds for the subjects’ own name and images of happy faces. Results from other

studies [45] suggest that subliminally presented pictures of angry faces may yield stronger emotional

responses compared with images of non-consciously perceived happy faces, especially in men. Some

of the apparent inconsistencies in results from experiments designed to influence emotional responses

through non-conscious stimuli have fed the feathers of those eager to dismiss such evidence altogether.

However, we must bear in mind that emotional cognition depends on a variety of epigenetic variables,

such as personal experience and culture, and that results can be expected to vary considerably as a

function of the latter.

Research on the influence of non-conscious perception on cognitive processes such as recognition,

memory, and learning harks back to the experimental studies by Marcel, who investigated effects of

visual masking on word recognition. These early findings [46] showed that conscious processing of

visual objects is not necessary for their subsequent recognition, motivating further studies on subliminal

semantic priming, where clearly visible targets are preceded by non-perceptible stimuli, so-called primes.

Non-conscious primes have been found to directly influence the conscious processing of supraliminal

targets. For example, near-threshold visual primes in a memory task significantly increases the recall

of items that are not recalled when presented without the primes, despite the fact that the reported

“feeling of knowing” of observers did not change between the two experimental conditions [47].

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Non-conscious processing therefore effectively supports conscious representation without individuals

being aware of the immediate behavioral outcome. In experiments where subjects had to classify visually

presented words (targets) into semantic categories, significant effects of semantically congruent

non-conscious primes, producing significantly lower error rates, were reported [48]. The prime words

were rendered undetectable through masking and brief exposure durations between 17 and 50 ms, and

observers were instructed to respond within a narrowly restricted time window. The magnitude of

priming effects as a function of prime visibility [49] has been investigated using linear regression

analysis, showing that conscious semantic representation is particularly facilitated by non-conscious

primes, suggested by the results of a multitude of studies on memory without awareness [50,51].

Neurophysiological studies have provided insight into the brain correlates of semantic priming, using

a combination of behavioral task and brain-imaging technique [51]. It was shown that non-conscious

prime stimuli have a measurable influence on the electrical and hemo-dynamic characteristics of brain

activity. Other functional neuro-imaging studies have investigated brain correlates of the so-called “mere

exposure effect” [52–54]. The latter describes observations where mere pre-exposure to visual objects

that are not identifiable beyond the chance level is sufficient to significantly influence subsequent

preference and memory recall of consciously perceived objects. The “mere exposure effect” may thus

be seen as a variation of subliminal semantic priming since it suggests, like priming effects in word

recognition, that non-conscious processing impacts on conscious memory judgments. In groups of

subjects making memory and preference judgments about consciously perceived objects after previous

exposure to subliminal stimuli, specific neural activities in the right lateral prefrontal cortex associated

with the implicit memory retrieval process were identified [55]. The data appear consistent with

earlier evidence for right lateral prefrontal activation during implicit behavioral guidance without

awareness [56], and have been interpreted in terms of a particular memory system operating outside

consciousness. Subjects were not aware that they had been exposed to their preferred or correctly

recalled objects before, whereas their brains had processed the subliminal information effectively.

Associative learning without conscious report has been tagged by specific temporal patterns of

event-related potentials (ERP). ERP activities triggered by aversive responses (shock-versus-no-shock

aversive conditioning) to non-consciously perceived faces were compared to activities triggered by

aversive responses to consciously processed faces [57]. Specific temporal activity patterns indexing the

acquisition of a conditional response to the non-consciously processed faces were found, supporting

the idea that brain traces of classical conditioning are formed in circuits that control non-conscious as

well as conscious behavioral processes or experience. Visual perceptual learning experiments have

shown that subliminal presentation of one of two contingent signals in a choice reaction time task

yields the same learning performance as presentation of two consciously perceived contingent signals

while subjects were unable to recall the nature of the non-consciously induced contingencies after

learning [58]. Similarly, non-consciously induced auditory affirmations embedded in soft background

music have been found to influence the learning and conscious recall of semantically ordered lists [59].

Subjects who were exposed to subliminal voice input did significantly better in recalling items from

the lists than controls.

Evaluative conditioning is a particular case of emotional priming. Changes in emotional responses

to stimuli that are supposed to be affectively neutral at the beginning can be primed in either a positive

or negative direction, as in the controversial experiments by Underwood mentioned earlier here, by

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introducing a subliminal associative stimulus. After repeated association with stimuli carrying strongly

negative or positive emotional connotations, the initially neutral stimuli then elicit emotionally biased

responses. Some studies using evaluative conditioning have shown that the conscious evaluation of

objects judged “neutral” at the beginning changed towards “negative” or “positive” judgments after a

series of trials where the presumed neutral objects have been associated repeatedly with either a

positive or negative, non-consciously perceived stimulus [60]. Such observations have been interpreted

in terms of subliminal contingency learning through interactions between non-conscious emotional

responses and conscious decisions about “good” and “bad”, or values and norms in general. Whether

or not non-consciously perceived emotional stimuli suffice to produce reliable, firmly consolidated

contingency learning has been put into question by results from more recent experiments. For example,

item-based analyses of responses to individual stimuli from several experiments have led to the

conclusion that consistent evaluative conditioning only emerges when, in the course of the learning or

valence acquisition process, subjects are made aware of the nature of the contingency between a

neutral stimulus and an emotionally biased, positive or negative, associated stimulus [61]. Weaker

effects from previous studies with merely subliminal contingencies [60] may partly be explained by

factors such as inter-individual differences in attention or readiness to respond. However, valence

acquisition through repeated contingency priming is a rather particular learning process, where initially

undetermined or ambiguous emotional representations can shift towards strongly biased ones in either

of two strictly opposite directions. To achieve stable output from such learning may require conscious

control at critical moments, and the more recently reported necessity of momentary contingency

awareness [61] may reflect a mechanism that fulfills an important functional role in the consolidation

process, as will be explained in the following chapter in the light of the model proposed here.

Accounting for the effects of non-conscious sensory stimuli on conscious behavior requires making

a clear distinction between the sensory threshold, that is the psychophysical or statistical threshold for

the detection of a stimulus as defined by Signal Detection Theory [62], and other thresholds for the

semantic processing of stimuli, such as recognition or identification thresholds. A subliminal sensory

signal or stimulus is defined as a signal with intensity levels below the psychophysical detection

threshold. During exposure to a psychophysically subliminal stimulus in a visual task, a human observer

may sometimes be aware of the fact that he/she may have seen something, but will not be able to say

what it was, or be unaware of other specific characteristics. The influence of subliminal signals on the

spatial and temporal integration of contrast stimuli has been investigated psychophysically for a long

time [63,64], showing that non-conscious signals influence conscious vision. Electrophysiological

studies have shown significant event-related brain responses to subliminal visual stimuli [65], where a

specific signal component could be assigned to the processing of a non-conscious visual target.

Evidence for a shift from non-conscious to conscious sensory processing as a function of visual

context has been found in psychophysical experiments with supraliminal contrast lines and subliminal

contrast targets collinear with the lines. In these experiments, small vertical contrast lines (targets) had

to be detected at fixed locations. In some conditions, the targets were presented together with a clearly

visible, spatially separated collinear line (context); in others, the targets were presented alone (no

context). While the contrast intensities of these targets were mostly subliminal, or non-detected

without the context, they became detectable when presented with the context [66–68]. Subliminal color

targets were also found to become detectable when presented together with consciously perceived

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colored lines or edges, but needed longer exposure durations for the effect to occur compared with

achromatic versions of the same stimuli [69,70]. Brain correlates of this phenomenon have been

identified in the visual cortex of a wakeful behaving monkey accomplishing a similar psychophysical

detection task [71], where neural activities triggered by targets were found to be increased by the

presence of a clearly visible, spatially separated, collinear line, and diminished by the presence of a

perpendicular line. These studies have led to identifying the underlying neural mechanisms in terms of

long-range interactions, suggesting that the latter may be involved in generating interactions between

conscious and non-conscious visual signals.

However, neural pathways other than those projecting to striate cortex seem to be involved in

generating the non-conscious processing of visual signals. In patients with cortical blindness caused by

lesions to their primary visual cortex (striate cortex V1), residual responses to visual objects are found

while observers are unable to report what they actually see [72]. Such patients accurately detect

monochromatic visual stimulus patterns, can discriminate direction of movement as well as orientation

of stimuli in their “blind” fields, and are able to discriminate the wavelength of chromatic stimuli in

the absence of any consciously acknowledged perception of color [73]. Whether the loss of all

conscious vision is an inevitable consequence of striate cortical destruction has remained unclear.

Patients with homonymous right hemianopias tested in tasks designed to assess their perception of

visual objects presented within the blind field were capable of making appropriate preparatory manual

adjustments (reaching and grasping) and seemed able to consciously process structural and semantic

characteristics of such objects [74]. Monkeys with unilateral removal of V1 preserve residual visual

capacity in the sense that the animals can still detect and localize visual signals in their affected

hemifields, but do not seem to be able to identify the nature of these signals [75]. Non-conscious visual

processing thus influences conscious action in humans [76] as well as animals.

3. The Functional Role of Non-Conscious Representation

Non-conscious brain processes are presumed to have the capacity of processing a majority of

incoming signals and to hold them available for further processing, after selection, at the conscious

level, which is limited in capacity [10,12,13]. Visual search studies have shown that observers search

faster and are more efficient when they are not conscious of what they need to be looking for [77]. It

also has been shown that non-conscious information processing is not only faster, but also capable of

generating multidimensional knowledge of interactive relations between variables that are too

sophisticated to be processed consciously [78]. A great deal of human decision making in everyday life

occurs indeed without individuals being fully conscious of what is going on, or what they are actually

doing and why. Also, human decisions and actions based on so-called intuition are quite often timely

and pertinent and reflect the astonishing ability of the brain to exploit non-conscious representations

for conscious action, effortlessly and effectively. Non-conscious representation is aimed at reducing

complexity at the level of conscious processing. It enables the brain to select, from all that it has learnt

about outer and inner events, only what is needed for producing a meaningful conscious experience.

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3.1. Adaptive Resonance and Brain Learning

Adaptive resonance theory [14] conceives the brain as a knowledge generating machine with

multiple, parallel distributed unit structures. It has given valuable conceptual support for thinking

about how different processing levels may produce coherently organized knowledge structures, how

context-sensitive adaptive learning may generate non-conscious representations, and how these

latter can be made available to conscious experience at a given moment in time, generating

meta-representations of knowledge that become embedded in a single conscious experience. In neural

networks, cells can become subliminally active when they receive priming signals that sensitize or

modulate their actual response or responsiveness by preparing them to react more quickly and

vigorously to subsequent bottom-up inputs that match the priming signals [79]. Perceptual knowledge

of a visual environment, for example, would require that subliminal mechanisms be present in every

cortical area wherein learning can occur, since without such mechanisms, any learned knowledge

would be rapidly degraded and subject to what Grossberg [14] refers to as “catastrophic forgetting”.

Neural network models specifically developed to account for subliminal priming effects [80] suggest

modifications of neural reaction times to subsequent inputs, according to whether or not there are

traces of subliminal processing of earlier input. Such models use parallel processing modules, or cell

assemblies, with different lateral connectivity and output functions. Their functional properties are

consistent with the hypothesis that the human brain uses parallel codes for the representation of

contents or knowledge, and that these codes generate a conscious state when the discharges of

functionally related neurons match in the domain of knowledge and in the domain of time.

Non-conscious brain mechanisms would serve the purpose of boosting relevant bottom-up signals and

suppressing irrelevant signals at the appropriate time, and thus lead to a constant updating of current

representational knowledge outside consciousness. Temporal summation at dendrites of hippocampal

neurons in the rat [81], obtained with a technique where the strengths, sites, and timing of dendritic

inputs can be controlled with precision, reveal that the temporal integration of synaptic inputs can

readily switch between subthreshold and suprathreshold summation. This seems to suggest that active

conductance in concert with passive cable properties in biological neural networks may serve to boost

coincident synaptic inputs and to attenuate or suppress non-coincident inputs. Such properties of

synaptic transmission could be exploited by brain mechanisms to generate interactions between

specific, temporally related subliminal and supraliminal signals.

Earlier cognitive theories had suggested that perceptions and sensations may feed into functionally

separate processing streams, operating within or outside consciousness [7,82]. Kihlstrom [6], in

particular, suggested that conscious processing is functionally dissociated from perceptive-cognitive

functions such as discriminative responses to sensory input, perceptual skills, memory, and higher

mental processes involved in decision making, judgment and problem solving. On this basis, he

proposed taxonomies for what he referred to as “the cognitive unconscious”. Kihlstrom emphasized

that humans seem to be able to perform cognitive analyses on information which is not itself accessible

to awareness by means of automatic and unconscious procedural knowledge. He suggested a tripartite

division of the “cognitive unconscious” into “truly unconscious”, “preconscious”, and “subconscious”

parallel processes. These three would run in parallel with a “truly conscious” processing stream that

generates declarative knowledge structures. Kihlstrom’s theory suggests four parallel processes to

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account for the ways in which the brain generates knowledge. Mechanisms that would explain how the

brain passes from one level to another are not suggested.

The idea of a strict functional segregation between the cognitive unconscious and conscious

experience may have to be reconsidered. The brain appears to process information through circuits

which interact at multiple levels of integration and across large distances in the brain, well beyond

intrinsic functional specialization [83–87]. It seems plausible to suggest that subliminal perceptual

input is processed and represented in all areas of the brain capable of generating resonant interactions,

where subliminal representations are made temporally available to conscious experience on the basis

of mechanisms detecting coincident representations. Representations embedded in conscious

experience can then also be temporally suppressed on the basis of these same mechanisms. One of the

problems with such a conceptual framework consists of explaining how subliminal input traces can be

processed and stored in neural structures without interfering with ongoing processing or, more

importantly, without destroying or changing representations that are already stored.

3.2. Non-Conscious Representation Matching

Attempting to solve this problem, Grossberg [14] defined specific functional principles for the

generation of non-conscious representations in resonant circuits of the brain. These functional

principles exploit two mechanisms of neural information processing, referred to as bottom-up

automatic activation and top-down matching.

(1) Bottom-Up Automatic Activation is a mechanism for the processing and the temporary

storage of perceptual input outside conscious experience. Through Bottom-Up Automatic

Activation, a group of cells within a given neural structure becomes supraliminally active

whenever it receives the necessary bottom-up signals. These bottom-up signals may or may

not be consciously experienced. They are then multiplied by adaptive weights that represent

long-term memory traces and influence the activation of cells at a higher processing level.

Grossberg [14] originally proposed Bottom-Up Automatic Activation to account for the way

in which pre-attentive processes generate learning in the absence of top-down attention or

expectation. It appears that this mechanism is equally well suited to explain how subliminal

signals may trigger supraliminal neural activities in the absence of phenomenal awareness.

Bottom-Up Automatic Activation generating supraliminal brain signals, or representations

with adaptive weights near or at zero, would be a candidate mechanism to explain how the

brain manages to process perceptual input that is either not relevant at a given moment in

time, or cannot be made available to conscious processing because of a lesion in the circuitry,

as in vision without consciousness for example.

(2) Top-down Representation Matching is a mechanism for selectively matching bottom-up

representations of incoming signals to learnt memory representations. Subliminal

representations may become supraliminal when bottom-up signals or representations are

sufficiently relevant at a given moment in time to activate statistically significant matching

signals. These would then temporally match the bottom-up representations (coincidence). A

positive match confirms and amplifies ongoing bottom-up representation, whereas a negative

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match tends to invalidate ongoing bottom-up representation [14]. Top-down matching thus

may be conceived as a selective process where non-conscious representations become either

embedded in, or remain temporarily inaccessible to, conscious experience.

The matching rules address the so-called attention-pre-attention interface problem [14] by allowing

pre-attentive (bottom-up) processes to use some of the same circuitry that is used by attentive (top-down)

processes. This would help stabilize cortical development and learning. Top-down matching in its most

general sense generates feed-back resonances between bottom-up and top-down signals to rapidly

integrate brain representations and hold them available for a consciousness experience at a given moment

in time. Non-conscious semantic priming can be explained on these grounds. Statistically significant

positive top-down matching signals produced on the basis of strong signal coincidences would explain

why subliminal visual representations become consciously perceived when presented simultaneously

with a specific context, especially after a certain amount of visual learning or practice [88]. Conversely,

significant negative matches produced on the basis of repeated discrepancies generating strong negative

coincidence signals could explain why a current conscious representation is suppressed and replaced

by a new one when a neutral conscious representation is progressively and consistently weakened by

association with a strongly biased representation, as in evaluative conditioning and contingency

learning [60,61]. The above mentioned functional properties require long-range connectivity of cortical

circuits capable of generating what Edelman [4] called “reentrant signaling”. Bottom-up representations

activating specific structures of such circuits, but not producing sufficiently strong matches to

long-term memory signals, will remain non-conscious. Strong positive top-down matching of selected

representations will compete with weaker or negative matches and, ultimately, produce their

suppression from an ongoing conscious experience, as for example in psychodynamic suppression,

where sudden conscious integration of new input interferes with the ongoing conscious processing of

other stimuli. Also, specific instructions telling subjects what to expect or what to attend to can thereby

generate top-down expectation signals strong enough to inhibit matching of other relevant signals

at the same moment in time, as for example in the hypnotic control of physical pain. Strong negative

top-down matching reflects a competing process, generating output of the opposite sign, i.e., a negative

instead of positive coincidence index. Results from certain observations in motor behavior, which

operates mostly outside awareness [89], highlight potential implications of negative top-down

matching for conscious control in learning processes with conflicting intermediate output. For

example, it has been shown that individuals may become aware of unconsciously pursued goals of a

motor performance or action when the latter does not progress well, or fails [90]. This could reflect the

consequence of repeated negative top-down matching of the non-conscious bottom-up goal

representation and top-down expectation signals in terms of either memory traces of previous success,

or representations of desired outcome. Repeated and sufficiently strong negative matching signals

might thereby trigger instant awareness of important discrepancies between expectancy and reality. In

contingency learning where an expectedly neutral stimulus is repeatedly associated with a biased one,

conscious control might be necessary to reinforce and consolidate new representations of the neutral

stimuli. Subliminal exposure to a biased associative stimulus without contingency awareness might fail

to produce such consolidation because the negative matching signals may in this case not be strong

enough to outweigh the old representation. It is, indeed, likely that conscious control in any learning

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under conditions of high uncertainty fulfills an important adaptive function that has evolved in

response to pressure from a steadily changing environment.

4. How Does the Brain Link Non-Conscious Representations to Generate Conscious Experience?

Dresp-Langley and Durup [13] suggested that non-conscious representations are linked to conscious

experience through coincidences of neural activity patterns in resonant brain circuits. The term

representation is defined here as by Churchland [91] in terms of patterns of activity across groups of

neurons which carry information. Such patterns of neural activity are described by signals distributed

across time and forming unique sequences. They constitute the potential temporal signatures of

conscious experience.

4.1. The Temporal Signatures of Conscious Experience

Several approaches have suggested functional properties to explain how groups of neurons could

produce specific temporal signatures through timing-dependent mechanisms where bottom-up

processing is represented by the temporal firing activity of a specific coding assembly for a specific

temporal window or duration. The activity traces of long-term memory representations would then

consist of unique combinations of many such temporal sequences [15], generated within reentrant

circuits of neurons with widely extending long-range connections. Dresp-Langley and Durup [13]

proposed that, whenever such memory traces generate significant reentrant matching signals in the

dedicated resonant circuitry, a conscious experience is triggered, and its unique temporal signature is

“printed” in the brain. This signature remains potentially available for a new conscious experience, and

can be retrieved again through top-down matching.

John [12] suggested that a conscious experience may be identified with a brain state where

information is represented by levels of coherence among multiple brain regions, revealed through

coherent temporal firing patterns that deviate significantly from random fluctuations. These

assumptions are consistent with the idea of stable and perennial temporal signatures of conscious

experience. These latter arise from temporal interactions between non-conscious representations and

are preserved when spatial remapping or cortical reorganization takes place. Empirical support for this

theoretical framework comes from evidence for functional links between electroencephalographic

activities and consciousness [92]. A temporal activity index signaling coherent firing patterns

(coherence index) was computed, and found to change significantly with increasing sedation in

anesthesia, independently of the type of anesthetic [93] Decreasing temporal activities were reported

when doses of a given anesthetic were increased. Characteristic temporal activity patterns signaling

coherence occur across brain regions during focused arousal and during REM sleep, when the subject

is dreaming [94] They disappear in dreamless, deep slow-wave sleep, which is consistent with the

findings on deeply anesthetized patients, suggesting that the temporal brain signatures of conscious

experience are activated in dreaming, which is consistent with [95], who suggested earlier that dreams

and conscious imagination represent equivalent conscious experiences.

The temporal activity matching of non-conscious representations for the generation of conscious

experience results from intra-cortical reverberation and may correlate with brain mechanisms which

establish arbitrary but non-random departures from different functional regions or topological maps,

Brain Sci. 2012, 2

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which may be subject to functional re-organization. Thus, conscious experience is constructed on the

basis of selective matching of non-conscious representations. This requires reentrant brain circuitry,

long-range inter-cortical connectivity and, most importantly, functional plasticity. Such brain

properties should make it possible to retrieve any given temporal signature through any set of coding

cells. The neural basis of conscious experience is then identified with specific temporal properties of

resonant activity patterns, arbitrarily determined through brain learning.

4.2. Functional Implications of Long-Distance Reentrant Signaling

Reverberant circuits or loops in the brain have their own intrinsic functional topology [96,97] and

were found in thalamo-cortical [98] as well as in cortico-cortical pathways [99,100]. Reverberant

neural activity, or reentrant signaling, is a purely temporal process that generates feed-back loops in

the brain. It reflects an important functional property of the brain because without it, the conscious

execution of focused action would be difficult, if not impossible [101]. This has led to suggest that

consciousness relies on the extension of local brain activation to higher association cortices that are

interconnected by long-distance connections forming reverberating neuronal circuits extending across

distant perceptual areas. A major functional advantage of such long-distance reverberation would be

that it may enable the neural traces of non-conscious representations formed in functionally specific

circuits to travel well beyond their functional boundaries. Functional imaging studies have associated

conscious brain activity with the parieto-frontal pathways, others suggested occipital correlates [86,87].

What both these brain regions have in common, interestingly, is that they are protected from fluctuations

in sensory signals and therefore allow information sharing across a broad variety of higher cognitive

processes. We argue that such selective information sharing leads to a significant reduction in

bottom-up signal variations, which provides a clear functional advantage for the top-down matching of

non-conscious representations at the least possible cost in terms of information processing. Sorting out

highly complex cross-talk between signals from a multitude of different sensory channels is then no

longer necessary. Moreover, long-distance reverberation of neural activity traces across long-range

connections enables the functional segregation of spatial contents from their temporal traces, which

clarifies how a stable and precise brain code can be generated despite the brain’s highly plastic and

largely diffuse spatial functional organization and thereby resolves the stability versus plasticity

dilemma [14]. A candidate mechanism for explaining how this may work is signal de-correlation, an

important concept in neural network theory and systems theory in general. Signal de-correlation

reduces cross-talk between multichannel signals in complex systems while preserving other critical

signal properties and could therefore be an important aspect of selective brain processing, with an

undeniable adaptive advantage to any species having evolved such capacity [13].

4.3. Cortical Plasticity and Epigenetic Factors

A multitude of sensory, somatosensory, and proprioceptive signals can be perceived simultaneously

in a single conscious moment. The integration of such a variety of signals into a unifying conscious

experience originate relies on the temporal linking of non-conscious representations, which have to be

stable, yet, possess functional plasticity to enable the continuous updating of representations in

response to changes in context. This allows the brain to learn and integrate new facts, events, and event

Brain Sci. 2012, 2

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properties. Clinical observations and case studies of the “phantom limb” syndrome [102] are consistent

with the idea of a highly plastic functional organization of the brain. The phantom limb syndrome was

first mentioned in writings by Paré and Descartes, referred to and described in great detail by [103]. It

has been repeatedly observed in hundreds of case studies since. After arm amputation, patients often

experience sensations of pain in the limb that is no longer there. Experiments with such patients have

shown that about a third of them systematically experiences stimulations of the face as coming from

the phantom limb, with a topographically organized map that matches individual fingers of a hand.

Similar evidence for massive functional re-organization of somatotopic maps after digit amputations

has been reported since. For example, several years after dorsal rhizotomy, a region corresponding to

the hand in the cortical somatotopic map of the adult monkey brain can be activated by stimuli

delivered to the face [104]. It has been suggested that cortical remapping should be possible

everywhere in the higher brain, and massive functional plasticity [105] would explain how brain traces

of non-conscious representations remain available to conscious experience, even when the original

circuits which have built them are destroyed.

It seems that during brain learning, the progressive selection of coincident activity traces of

non-conscious representations builds some kind of access code for conscious experience. This is

achieved on the basis of purely statistical criteria and progressively leads to fewer and fewer

consolidated patterns for the increasingly complex signal coincidences the brain is to learn throughout

its epigenetic development. When we are born, all brain activity is more or less arbitrary, but not

necessarily random. During brain development, temporal activity patterns elicited by events in

biophysical time will be linked to a variety of particular conscious experiences in a decreasingly

arbitrary manner. Frequently activated patterns are progressively consolidated through a process of

developmental selection [4,13]. The idea of developmental selection of temporal signatures of

conscious experience resolves a critical problem in Helekar’s model [15], which fails to explain how

the non-arbitrary linking of non-conscious representations could work. Helekar seemed to be aware of

this problem and proposed a genetically determined linkage which is, however, inconsistent with the

fact that brain learning is experience dependent and, despite universal principles and prewired

functions, strongly influenced by epigenetic factors. Helekar’s elementary, experience-coding temporal

activity patterns are generated by prewired subsets of neural patterns from all patterns the brain could

possibly generate. His hypothesis was that only patterns that are members of this prewired subset

would be involved in the generation of conscious experience.

I prefer to think that non-conscious representations are encoded and decoded in the brain through

mechanisms of neural learning which, although they may well be universal [106], express themselves

not through some genetic program, but on the basis of developmental processes which are themselves

experience-dependent. Such processes can ensure the non-arbitrary linkage of non-conscious contents

and their brain traces. Once such traces are matched to form the temporal signature of a new conscious

experience, this signature remains potentially available as a “brain hypothesis”. This hypothesis is then

is either progressively reinforced and consolidated, or slowly extinguished. Once consolidated, the

linkages between non-conscious representations become less arbitrary, in some cases deterministic.

Grossberg [11] himself often invoked evolutionary pressure to explain why resonant brain mechanisms

make good sense. Let us go one step further and suggest that evolution has produced brains capable of

generating conscious experience on the basis of a higher and more abstract level of functional

Brain Sci. 2012, 2

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organization than previously imagined, where spatial aspects of information processing are discarded

and only the temporal traces of non-conscious representations preserved to be matched for complex

conscious experiences at any given moment in time (Figure 1), with or without external stimuli.

Figure 1. The statistical selection of matched temporal activity traces of non-conscious

brain representations builds the neural signatures of conscious experience in biophysical

time. Psychological time associated with a conscious experience is subjective.

5. Conclusions

Non-conscious brain representations are the basis upon which all conscious experience is built. The

capacity of the human brain to generate such experience is a result of evolution, expressed through

continuous interaction between the brain and its environment from early childhood on, progressively

enabling conscious experience on the basis of the temporal matching of the neural activity traces of

non-conscious representations. These matching processes take place in physiologically determined

biophysical time, while psychological time associated with a conscious experience is entirely

subjective. The brain learning process which ensures the continuity and the stability of representations

and therefore that of conscious experience relies, as suggested by the model approaches discussed here

above, on the progressive development of dedicated resonant circuits capable of reentrant signaling and

space-time signal de-correlation. The latter ensures that the temporal activity traces of non-conscious

representations are maintained in the brain independently from functional specialization or spatial

cortical maps. The dedicated resonant circuits that are necessary to achieve this are progressively

and arbitrarily formed in the brain. Although their intrinsic functional properties are universal and

pre-wired, their expression strongly depends on epigenetic factors. The latter determines the amount of

Brain states

Conscious experience

Psychological time

Temporal activity traces of

non-conscious representations Neural signature of

conscious experience

Biophysical time

Brain Sci. 2012, 2

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long-range connectivity between neural structures activated by bottom-up signals at a given moment in

time, and distant structures not directly activated by bottom-up input. When a critical amount of such

long-range circuitry is consolidated, reentrant signaling will trigger conscious experience. This

happens whenever non-conscious representational traces statistically match the temporal signatures of

learnt and sufficiently stable long-term memory representations. Further investigation of experience

related temporal activities in the thalamo-cortical and cortico-cortical pathways of the brain might one

day allow tracing such mechanisms.

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